A very important and truly wonderful paper in Nature described a tour-de-force analysis of the Mammalian Evolutionary Record, and draws the following two important conclusions:

The diversification of the major groups of mammals occurred millions of years prior to the KT boundary event; and

The further diversification of these groups into the modern pattern of mammalian diversity occurred millions of years later than the KT boundary event.

The KT boundary event is the moment in time when a ca. 10 km. diameter object going very fast hit the earth in the vicinity of the modern Yucatan, causing the extinction of the dinosaurs (and almost everything else larger than a microwave). It has been suggested that this event resulted in (allowed for) the subsequent diversification of the mammals, presumably because the earlier extinction event opened up previously filled niches, into which the mammals evolved, and possibly because of dramatic climate change that occurred with this event.

One of the reasons that this study is important is that it seems to falsify this long-standing hypothesis.

This paper is thoughtfully discussed on Pharyngula and Sandwalk, and I recommend that you have a look at those sites.

I have a number of comments on this paper. Before I make them I want to say that I have absolutely no strong feeling on which of these ideas is either likely or important. I’m not coming at this with a particular agenda regarding this evolutionary pattern of mammal evolution. The KT boundary question is not directly in my area of research (I’m post middle Miocene). I do have one agenda-like perspective, however, that I want to lay out in the beginning: Larry Moran points out that the evidence for close connections between climate change and evolution seems to weaken with every new study, and that we have to simply start believing that the connection is a falsehood. I disagree with this conclusion, but in a way that is not meant to preserve the old “climate change – evolution” link. I agree with Larry that the link as I’ve ever seen it described and tested has failed to find support in the data. However, I do not believe it is correct to say that there is no relationship between climate change and speciation. I think that the way the link has usually been postulated is incorrect, and that when it comes to understanding the environmental change-speciation link we are dumb little babies (so far). I’ll discuss this in more detail below.

The following figure is from the Nature paper, and shows the new mammal phylogeny. The dotted circle is the KT boundary. Notice that the major taxa are shown to have emerged before the event, and the rise of numerous subsequent species after it. The lineages shown on this graph represent nearly every single living mammal, but no fossil species are used since this is a molecular phylogeny. Click on the figure to get a larger copy.

The (Possibly) Real Importance of this Paper

Never mind the KT event or the test of the hypothesis that mammalian radiations are linked to it. This paper provides what appears to be the best current phylogeny of the living mammals at the higher taxonomic level, significantly better than anything we have had before. One could argue about some of the details (one has to pick “a” tree for this kind of study, and there are alternative possibilities) and the resolution of the given tree is poor for the more recent radiations (I’m personally looking for the best current rodent tree and I’m afraid this one won’t do). However, attempts to put the major groups together have been difficult and often unsatisfying, so it is great to have a new, most up to date version.

However, the reader should not assume that this tree is the final accepted phylogeny of the mammals. Other research teams will come out with critiques and there will be revisions, I’m guessing sooner rather than later. Watch for it. What will be interesting is to see if the critiques involve the overall pattern described here in relation to the KT boundary.

I am not certain that we are ready to believe calibration of molecular phylogenies.

The timing of events on this tree are estimated by using molecular clocks calibrated by various bits of the fossil record. The authors were fairly careful in doing this, not using a single clock, but adjusting for suspected rate variations among different clades. The fossils give minimal dates for divergences …. so if you have a fossil that has an undoubted featured of a certain clade, and the fossil is dated, then you know that the split between that lineage and it’s nearest molecular relative predated that fossil date.

I have not done a thorough analysis of the supplemental data supplied with the paper, so please understand that I do not have a specific criticism of the way in which the molecular data are calibrated. My gut feeling is that the authors did a great job. However, I do have an overall problem with molecular calibration and I want to preach caution.

The initial diversification of the living superorders and orders is set in this study at 93 million years ago. An acceleration of diversification is set startling at the “Early Eocene” (the paper does not give a date for this, so I’ll set it at 54 million years ago).

Taking 65 million years ago (the KT event) as a benchmark, the earlier date would have to be moved towards the present by 43 percent in order to “fit” the data with the KT boundary. I other words, if you KNEW that the initial diversification happened at the KT boundary, then you would have to adjust all of your molecular data by 43 percent, or putting it yet another way, if all you had was the molecular phylogeny and the date of the KT event, you would have to have confidence in your molecular calibration sufficient to believe that you could not be wrong by 43 percent. Forty-three percent sounds like a lot.

I guarantee you that most molecular biologists will say that 43 percent is a very large number. I also guarantee you that a LOT of fossil people will say that 43 percent is NOT a large number, and that there have been many cases where the molecular calibration is off by a factor of two.

For example, over the period of several years, the molecular data for the split of humans and the other apes had the following pattern: In the 1970s, there was one group saying 5 million, other groups saying much more, like 6-7. Over time, the “long view” groups revised and revised until finally they were also saying something close to 5 million, or even a little less. Then a fossil was found in Ethiopia that dated to just under 5 million and it looked like a good candidate for an australopith at the boundary between a last common ancestor and early hominids. So everybody was pretty darn happy with 5 million years.

Then, suddenly, more fossils started to show up and now we are looking at likely hominids closer to 6.5 or even 7 million years. The hominid-ness of the earliest fossil is somewhat in dispute, but frankly, the nay-sayers are probably wrong … the hominid-ape split probably dates to between 6 and 7 million, closer to 7.

So, the calibration of the DNA systems used to date the human-nonhuman ape split, a topic that has received considerable attention, has a fudge factor of 30 or 40 percent, depending on how you look at it.

Now, some of you are already thinking: Right, sure, but the early date in this study (93 million years) must be based on dated fossils! You can’t move the molecular estimate of the timing of a split between lineages to a point in time AFTER the existence of fossils demonstrating the split! Yes, you would be correct about that. So now the question is, are the early diversifications (the ones around 93 million years) linked to fossils that demonstrate the split? Again, I have not looked at the specific cases used for this calibration, but I believe that there are fossils of early mammals, indicating these splits, dated to well before the KT event. However, the first appearances in the fossil record of terrestrial mammals is hard to estimate, and the earlier in time one looks the more likely one underestimates the age of these events. If anything, I would guess that the 93 million year date is an underestimate, and that these splits really happened a bit earlier.

Is the Eocene (and Later) Estimate for Diversification Wrong?

Let’s say that the 93 million year date is an underestimate by 15 percent. If we recalibrate the entire tree based on this guesstimate, then the later diversification (said in this paper to be Early Eocene) would move from 55 million years to 63.5 million years ago.

Eocene and later diversification is not about the KT boundary

If it is true that there is a post-Paleocene (Eocene and later) diversification of living mammals, then this does not mean that mammals did not diversify in the early Paleocene, just after the KT event.

Studies looking at just the fossils did not disappear on the publication of this paper. I’ll give you one very handy and excellent example: John Alroy of the Smithsonian has a paper looking at early appearances of mammalian taxa in North America in relation to time. The following figures are from his paper: http://www.nceas.ucsb.edu/~alroy/Paleocene.html

Figure 1. North American mammalian diversity, origination (new appearance) rates, and extinction rates through the late Cretaceous and Cenozoic. Data are based on multivariate ordination and standardized sampling of faunal lists. (a) Standing diversity. Y-axis is logged to show the lack of either a log-linear (exponential) or asymptotic (simple logistic) pattern; instead, an offset between two logistic curves at about 65 MYA is indicated. (b) Origination rates. (c) Extinction rates.

Figure 2. Trends through time in North American mammalian body mass distributions. All species falling into each 1.0 MY-long bin are considered. (a) Mean body mass. (b) Standard deviation of body mass.

These fossil dates do not require calibration in relation to the geological column … they ARE the geological column. There is no ambiguity about the relationship between a spike in mammal species novelty and the KT event, at least in North America (where the direct events of the KT event may have been the most severe, by the way). The conclusion from the molecular data appears to be incorrect from this perspective.

Is the Later Diversification a Later “Event” or an Artifact of the Pattern?

It is possible that for any molecular record of sufficient diversity (a record of several higher taxa) and time depth, there will emerge “waves” of diversification that are partly determined by actual splits between species and partly determined by the patterns of extinction such that the apparent timing of the diversification a) has little do to with the actual events and b) follows along behind the “present” in fits and starts. Let’s look at an example, at least of “a”.

Now, I’m not going to do the actual work on this, I’m just going to mentally walk you through it. Imagine we wanted to estimate the time of diversification of the dinosaurs from the molecular data. We determine the clade of living forms that includes all possible dinosaurs. This would be the Archosauria, which includes the dinosaurs, the birds, and the crocodiles. Unfortunately, since we are basing this on living forms (using DNA) we can only sample the crocodiles and the birds, no dinosaurs.

The resulting analysis would show an initial diversification (the bird/croc split) way earlier than the presumed dinosaur radiations (I’m assuming there were multiple!) and another, much later radiation (the birds). We would be like the three statisticians hunting rabbits … we might be able to convince ourselves that we hit the rabbit, but the rabbit would be laughing at us.

It seems to me that the fossil record shows a diversification of mammals hard on the heels of the KT boundary, and the living mammal molecular reconstruction either has some calibration issues or is tracking a different phenomenon. Or both.

Even if the later radiation is “the” radiation… was KT unimportant? (Is environmental change really unrelated to speciation?)

This is a bit of a philosophical question, but it gets to the issue I mention above about the relationship between climate change and speciation. Larry is not going to like this, and I heartily look forward to his comments if he has chance to make some.

Free oxygen in the atmosphere is essential to much life on this planet. But it did not always exist. Had the biological processes that resulted in atmospheric oxygen not happened, all of the organisms that depend on it today would not exist. So, that ancient event – a clear example of environmental change — has a lot to do with all later evolution.

That is a very indirect link, making it trivial to the question of a connection between environmental change and speciation.

In terms of numbers of species as well as biomass, living ungulates mainly depend on widespread grasslands. Widespread grasslands emerged as a feature of the environment during the Miocene. The radiations we see of ungulates could not have happened were it not for the appearance of these grasslands (an environmental change). That is a less trivial link. It is not likely (as has been attempted) to find specific events … a particular dessication event, the closure of the Panama land bridge, etc. etc. to a particular radiation of the ungulates. And there is more than one radiation, likely. But the grass-ungulate link is less trivial than the oxygen-nearly everything link.

The rise of a particular evolutionary novelty and a particular climate event or environmental change is perhaps unlikely to have happened, and if it did, it would be hard to see. The history of speciation is not clearly linked to specific environmental changes to the extent that would be necessary for this to be our main explanation. This is complicated by the fact that many of the major “events” we see are rare, but we know that at least in the last few million years (and probably at various other longish periods of time in the past) orbital geometry running on cycles of tens of thousands of years has to be accounted for. But there is a very large scale link, and sometimes that link is closer and better fit historically and functionally than other times.

It is wrong to say that “environmental change causes speciation” and leave it at that. But it is also wrong to say that “environmental change is unrelated to speciation,” because there is a range of “trivial” to more direct connections between environments and adaptive patterns. I believe that we are not in a position to describe a pattern or to develop a strong theory in this regard at this time. Persistent belief in a simple environmental change-speciation link has probably, in retrospect, wasted a lot of our time and energy, but that is how science works. We need to move on towards a more nuanced and meaningful set of models.

It was the Birds Fault!

OK, so let’s say the fossil record is wrong, and we must simply believe the molecular record. Mammal radiation did not occur right after the KT boundary. Why?

Well, I want to re-emphasize that it probably did, so “why” may not be a valid question. However, there is one thing I’d like to throw into the works. I am about to make a number of enormous logical leaps, so hang on to the safety rope.

Some clades experience increase in body size over time. This does not necessarily mean that small forms disappear, but rather, the range of body sizes across species in a clade increases. In a way, you can think of this as diversification of potential niches, because (at least for terrestrial mammal) there is a link between body size and several important aspects of “niche” running from diet to predator-related issues to nesting, etc. So one thing you might expect is for there to be a link between increase in range of body size and increase in species diversity.

One system that may drive body size increase is the predator-prey relationship, whereby prey “outgrow” various predators, but predators also increase in size, over evolutionary time. It seems that dinosaurs at various time and places experienced predator-prey “arms races” in body size. It seems that this also happened with mammals.

Now, in the Paleocene, after the KT boundary, it is my understanding that few large (like, mammoths and such) critters were to be found, and that terrestrial ecosystems were dominated by largish avian predators. These Killer Big Birds (much like the Big Bird from Sesame Street but with a larger beak and a much coarser attitude) were probably the main predator on early post KT terrestrial mammals. But it seems (and I may be totally wrong here) that there was not an arms race for body size. Maybe a little one, but the mammals did not grow enormous during this period. That was to occur later, starting in the Eocene.

Why? Well, my hypothesis is this: Growing large has costs and benefits, but other adaptations do as well. The costs of growing large include slower reproductive rate and greater vulnerability in relation to the food supply, for instance. What if mammals that were being preyed on by Big Bird were able to adapt to this predation in a different way than getting larger? There are of course many ways to adapt to predators other than to outgrow them, and even when we do see large body size emerging we also see other things happening at the same time (like being fast, being cryptic, or being hard like a walnut).

Specifically, I hypothesis that the benefits of large size after subtracting the costs of large size were less than the benefits of some other strategy, and that strategy is one that would only work for a mammal being eaten by a bird. Perhaps the slightly different thermodynamics of mammals and birds was exploited, different diurnal patterns of energetics, or locomotory patterns. Fill in the blank: Mammals, with the special mammal feature of X reduced predation by birds, who were limited by Y by using strategy Z, such that Z is NOT increase in body size.

When Big Bird was replaced by mammalian predators, then we have mammal preying on mammal, and this discordance between X and Y (allowing for adaptation Z) did not apply. Large body size still has it’s benefits, and that becomes a major mode of adaptation, so we see the Eocene beginnings of a mammalian radiation involving body size increase and diversification of species. (This could also explain why rodents have not all grown to be larger than snakes and hawks.)

ADDED LATER: There is an excellent discussion of this research on Panda’s Thumb.
______________________________________________________________________________Sources:

Alroy, John. nd. The Fossil Record of North American Mammals: Evidence for a Paleocene Evolutionary Radiation. http://www.nceas.ucsb.edu/~alroy/Paleocene.html

Comments

Then I’ll repost my comments, too, after pointing out more recent developments.

Firstly, this paper has been published. It shows that molecular dating results in divergence date estimates that are much closer to what the fossil record suggests if people understand their calibration points, if those points are evenly enough distributed across the tree (both young and old, both inside and outside the clade of interest; Brochu 2004, 2005) and if at least some calibration points have not only minimum but also maximum ages. Maximum ages can be derived from the fossil record when a clade that should be present is absent from a formation with a very good fossil record. When no maximum ages are used, most estimates become too old.

Bininda-Emonds et al. made lots of blunders with their calibration points (see below) and didn’t use maximum ages at all, except that they fixed the age of the root, which is hardly defensible because the fossil record around it is quite poor.

Secondly, this paper shows that, of the wide diversity of known Cretaceous eutherians, not one is a placental. (OK, Schowalteria might be, but it’s a taeniodont, and no taeniodont has ever been in a phylogenetic analysis, as far as I know.)

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Number 11 at Pharyngula:

That’s the message of a new paper in Nature that compiled sequence data from 4,510 mammalian species

No, they did not.

They took the literature, compiled a supertree from the (hopefully) phylogenetic analyses they found there, got sequences of 66 genes for as many mammals as possible, and then used those sequence data plus 30 calibration points to estimate some divergence dates on that supertree.

That’s right: apart from its size, it’s just yet another attempt at molecular dating.

And not a very good one. The age of the basal divergence (between the monotremes and the rest) was fixed at a rather arbitrary date out of the range of ages the oldest known fossil on the monotreme side of the split could have. The other ages were only used as minimal ages; maximal ages were not used, thus providing no protection against too old divergence date estimates. Of course maximal ages cannot be derived from the fossil record as easily as minimal ages, but the fossil record from some epochs is good enough to let us interpret absence of evidence as evidence of absence with more than 50 % confidence.

There are only three outgroups, increasing the risk that the lengths of these branches could have detrimental effects on the branch lengths in the ingroup…

No, it is not an earth-shattering paper, despite having been published as an “Article” (rather than “Letter”) in Nature.

Number 15 at Pharyngula (where I give a link to the supplementary information of the paper, which is free-access; also, Diacodexis pakistanensis is now Gujaratia pakistanensis):

– Monotrematum is probably not a crown-group monotreme. Thus, Monotremata may be younger than 63.6 Ma.
– Tribosphenomys is far from being a crown-group rodent! Rodentia (unlike Rodentiamorpha) is younger than 57.25 Ma (…and I wonder where they got such a precise date…). Note that the reference Bininda-Emonds et al. cite makes this quite clear (it coins the name Rodentiamorpha).
– Not that I knew anything, but I’d be quite surprised if Eodendrogale were a crown-group scandentian. Thus, the crown-group of Scandentia may well be younger than 44.5 Ma.
– Same for Dendrotherium being a crown-group dermopteran.
– The genus Tarsius is 44.5 Ma old? Difficult to believe. I’d say a name change is in order.
– Diacodexis is a paraphyletic series of species around the base of Cetartiodactyla (which means that at least some of those species should get new genus names). Putting “Diacodexis sp.” into Suiformes does therefore not look defensible to me, but I’ll try to find the reference.
– Obviously, Pakicetus is not a crown-group whale. The crown-group of Cetacea (Autoceta) is much younger.
– Eomanis is far from a crown-group pangolin…
– I’d be very surprised if Ageinia turned out to be a crown-group bat. Thus, chances are high that the crown-group of Chiroptera is younger than 52.2 Ma.
– I’d be surprised if Riostegotherium turned out to be a crown-group dasypodid. But that’s outside my area of knowledge.
– The crown-group of Tubulidentata consists only of Orycteropus. Obviously Myorycteropus can’t be part of that…
– Nortedelphys was indeed described as a didelphimorphian, but I don’t buy it. It’s “the tooth, the whole tooth, and nothing but the tooth” (as usual in the Mesozoic). In any case, considering it a crown didelphimorphian really stretches it.
– Paucituberculata… all extant paucituberculates are caenolestids, and the fossil is most likely not one of those…
– I bet the fossil notoryctid is outside the crown-group.

Much sloppier work than I imagined.

Just for the record, I stand by that latter remark.

Comment 18 at Pharyngula:

and my point is that seeing a mammalian radiation prior to the K/T boundary should not be a surprising result —

But a placental and a marsupial radiation in the Cretaceous areNortedelphys and a few more problematic crumbs), no matter how common the remains of other mammals are, and no matter how small those are.

Comment 23 at Pharyngula (note that, in addition to the two isolated teeth, Monotrematum is also known from at least one small nondescript jaw fragment):

David – is there another use of the term “crown” in the picture?

No. For example, you’ll see they put divergence between Tachyglossidae and Ornithorhynchidae ( = the origin of crown-group Monotremata) very shortly after the K-Pg boundary; clearly the Paleocene Monotrematum was considered an ornithorhynchid (or a tachyglossid, but there’s no way to compare two isolated teeth to an echidna, so they clearly didn’t do that).

Comment 41 at Pharyngula:

Wow, that is a huge mistake. Are we sure they weren’t using Pakicetus to give a minimum age for the divergence of the Cetecea *stem* group? That would make a lot more sense.

Yes, but look at the tree: they put the divergence between baleen whales and toothed whales into what seems to be the Eocene. Or have a look at their calibration point for Monotrematum, the only known Paleocene monotreme — the divergence between Tachyglossidae and Ornithorhynchidae is right after the K-Pg boundary, fitting the age of Monotrematum, so Bininda-Emonds et al. seem to consider M. an ornithorhynchid.

This study would be more impressive if they had compared the crown group frequency to some kind of null model.

I agree.

Note how little time passed between reception and acceptance (just over 3 months) and between acceptance and publication (just under 2). That’s very fast.

[…]

Proto-placentalians may have been minor members of the fauna, as Mr. Marjanovic indicates, but they still could have been divided into several lineages that gave rise to different modern placental orders after the age of the dinosaurs.

This is of course correct; neither the fossil record nor our current knowledge of it are complete. But have another look at the tree: I count not two, not five, not ten, but forty-two lineages of Cretaceous placentals and marsupials, and those are just those that happen to have left extant descendants. That so many lineages were present in the Cretaceous but are so far absent from the fossil record is not probable. (I can’t do the math off the top of my head, but it can be done — a paper has recently been submitted which does something like this for amphibians.)

Comment 42 at Pharyngula (note that the echidnas = tachyglossids do have a fossil record in Australia that reaches back to the Miocene):

I should have mentioned that the only certain fossil ornithorhynchids are Miocene and younger. There are no known fossil tachyglossids (apparently the group evolved in the underexplored New Guinea). There are no known fossil monotremes from the Eo- or Oligocene (or for that matter the Late Cretaceous… there are several from the Early Cretaceous, however). Thus, Bininda-Emonds et al. have obviously used Monotrematum to calibrate the divergence between Ornithorhynchidae and Tachyglossidae.

Comment 54 at Pharyngula:

[…]

The latest word on the gastornithids — Diatryma is a junior synonym of Gastornis — is that they were herbivores, eating e. g. palm hearts.

[…]

Comment 2 at Sandwalk:

You are right that it was not a good idea to fix the age of the root at 166.2 Ma, and that the cladogenesis may well have happened earlier. However, most of the other calibration points are too old because the phylogenetic positions of the fossils in question were misinterpreted. Bininda-Emonds et al. regularly mistook stem-group representatives for crown-group members. For example, the one they took as the oldest rodent is the oldest rodentiamorph, as the paper they cite makes clear — Rodentia is younger than that, and Rodentiamorpha includes Rodentia plus its closest extinct relatives. For more, please see my comment over at Pharyngula: [URL deleted — see top of this comment]

This miscalibration pushes most, maybe all, divergence dates too far into the past. I’m sure this more than offsets the effect of the probably too young root.

Using only minimal ages for the calibration points and no maximal ages may not have been a good idea either. There are rich Late Cretaceous mammal faunas which lack any trace of placentals or marsupials — in some of those cases I think absence of evidence should be regarded as evidence of absence of a radiation.